Voluntary running suppresses tumor growth through epinephrine- and IL-6-dependent NK cell mobilization and redistribution

Cell Metabolism

Volumn 23, Issue 3, 2016, Pages 554-562

  Pedersen, Line ^a   Idorn, Manja ^b   Olofsson, Gitte H ^b   Lauenborg, Britt ^a   Nookaew, Intawat ^c,d   Hansen, Rasmus Hvass ^e   Johannesen, Helle Hjorth ^e   Becker, Jürgen C ^f   Pedersen, Katrine S ^a   Dethlefsen, Christine ^a   Nielsen, Jens ^c   Gehl, Julie ^b   Pedersen, Bente K ^a   Thor Straten, Per ^b,g   Hojman, Pernille ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Mental Health Services CPH   (Denmark)

^c CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

^e GENTOFTE UNIVERSITY HOSPITAL   (Denmark)

^f UNIVERSITY HOSPITAL ESSEN   (Germany)

^g UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

adrenalin; cancer; epinephrine; exercise; exercise oncology; immune cells; interleukin 6; natural killer cells; Physical activity

Indexed keywords

ADRENALIN; INTERLEUKIN 6; EPINEPHRINE;

ADRENERGIC SYSTEM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INCIDENCE; CANCER INHIBITION; CELL MOTILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; LYMPHOCYTIC INFILTRATION; MALE; MICROARRAY ANALYSIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RUNNING; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; C57BL MOUSE; CANCER TRANSPLANTATION; CARCINOGENESIS; EXPERIMENTAL MELANOMA; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; CARCINOGENESIS; CELL LINE, TUMOR; EPINEPHRINE; FEMALE; INTERLEUKIN-6; KILLER CELLS, NATURAL; MELANOMA, EXPERIMENTAL; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; RUNNING; SIGNAL TRANSDUCTION; TUMOR BURDEN;

EID: 84960808676     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.01.011     Document Type: Article

References (34)

1. W. Aoi, Y. Naito, T. Takagi, Y. Tanimura, Y. Takanami, Y. Kawai, K. Sakuma, L.P. Hang, K. Mizushima, Y. Hirai, and et al. A novel myokine, secreted protein acidic and rich in cysteine (SPARC), suppresses colon tumorigenesis via regular exercise Gut 62 2013 882 889
2. R. Ballard-Barbash, C.M. Friedenreich, K.S. Courneya, S.M. Siddiqi, A. McTiernan, and C.M. Alfano Physical activity, biomarkers, and disease outcomes in cancer survivors: a systematic review J. Natl. Cancer Inst. 104 2012 815 840
3. A.B. Bigley, K. Rezvani, C. Chew, T. Sekine, M. Pistillo, B. Crucian, C.M. Bollard, and R.J. Simpson Acute exercise preferentially redeploys NK-cells with a highly-differentiated phenotype and augments cytotoxicity against lymphoma and multiple myeloma target cells Brain Behav. Immun. 39 2014 160 171
4. P. Brodin, T. Lakshmikanth, K. Kärre, and P. Höglund Skewing of the NK cell repertoire by MHC class I via quantitatively controlled enrichment and contraction of specific Ly49 subsets J. Immunol. 188 2012 2218 2226
5. J.C. Brown, K. Winters-Stone, A. Lee, and K.H. Schmitz Cancer, physical activity, and exercise Compr. Physiol. 2 2012 2775 2809
6. J.R. Carlyle, A.M. Jamieson, S. Gasser, C.S. Clingan, H. Arase, and D.H. Raulet Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors Proc. Natl. Acad. Sci. USA 101 2004 3527 3532
7. M. Catoire, and S. Kersten The search for exercise factors in humans FASEB J. 29 2015 1615 1628
8. P. Chen, O.A. Aguilar, M.M. Rahim, D.S. Allan, J.H. Fine, C.L. Kirkham, J. Ma, M. Tanaka, M.M. Tu, A. Wight, and et al. Genetic investigation of MHC-independent missing-self recognition by mouse NK cells using an in vivo bone marrow transplantation model J. Immunol. 194 2015 2909 2918
9. J.F. Christensen, L.W. Jones, J.L. Andersen, G. Daugaard, M. Rorth, and P. Hojman Muscle dysfunction in cancer patients Ann. Oncol. 25 2014 947 958
10. C. Dethlefsen, G. Højfeldt, and P. Hojman The role of intratumoral and systemic IL-6 in breast cancer Breast Cancer Res. Treat. 138 2013 657 664
11. S. Dimitrov, T. Lange, and J. Born Selective mobilization of cytotoxic leukocytes by epinephrine J. Immunol. 184 2010 503 511
12. W.H. Fridman, F. Pagès, C. Sautès-Fridman, and J. Galon The immune contexture in human tumours: impact on clinical outcome Nat. Rev. Cancer 12 2012 298 306
13. A. Glasner, H. Ghadially, C. Gur, N. Stanietsky, P. Tsukerman, J. Enk, and O. Mandelboim Recognition and prevention of tumor metastasis by the NK receptor NKp46/NCR1 J. Immunol. 188 2012 2509 2515
14. S.I. Grivennikov, F.R. Greten, and M. Karin Immunity, inflammation, and cancer Cell 140 2010 883 899
15. E. Gross, J.B. Sunwoo, and J.D. Bui Cancer immunosurveillance and immunoediting by natural killer cells Cancer J. 19 2013 483 489
16. P. Hojman, C. Dethlefsen, C. Brandt, J. Hansen, L. Pedersen, and B.K. Pedersen Exercise-induced muscle-derived cytokines inhibit mammary cancer cell growth Am. J. Physiol. Endocrinol. Metab. 301 2011 E504 E510
17. K. Imai, S. Matsuyama, S. Miyake, K. Suga, and K. Nakachi Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population Lancet 356 2000 1795 1799
18. L.W. Jones, and C.M. Alfano Exercise-oncology research: past, present, and future Acta Oncol. 52 2013 195 215
19. M.J. Kraakman, H.L. Kammoun, T.L. Allen, V. Deswaerte, D.C. Henstridge, E. Estevez, V.B. Matthews, B. Neill, D.A. White, A.J. Murphy, and et al. Blocking IL-6 trans-signaling prevents high-fat diet-induced adipose tissue macrophage recruitment but does not improve insulin resistance Cell Metab. 21 2015 403 416
20. J. Mauer, J.L. Denson, and J.C. Brüning Versatile functions for IL-6 in metabolism and cancer Trends Immunol. 36 2015 92 101
21. A. McTiernan Mechanisms linking physical activity with cancer Nat. Rev. Cancer 8 2008 205 211
22. S.I. Mishra, R.W. Scherer, C. Snyder, P.M. Geigle, D.R. Berlanstein, and O. Topaloglu Exercise interventions on health-related quality of life for people with cancer during active treatment Cochrane Database Syst. Rev. 8 2012 CD008465
23. W.E. Naugler, T. Sakurai, S. Kim, S. Maeda, K. Kim, A.M. Elsharkawy, and M. Karin Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production Science 317 2007 121 124
24. B.K. Pedersen, and M.A. Febbraio Muscles, exercise and obesity: skeletal muscle as a secretory organ Nat. Rev. Endocrinol. 8 2012 457 465
25. B.K. Pedersen, and L. Hoffman-Goetz Exercise and the immune system: regulation, integration, and adaptation Physiol. Rev. 80 2000 1055 1081
26. H. Rabinowich, P. Sedlmayr, R.B. Herberman, and T.L. Whiteside Response of human NK cells to IL-6 alterations of the cell surface phenotype, adhesion to fibronectin and laminin, and tumor necrosis factor-alpha/beta secretion J. Immunol. 150 1993 4844 4855
27. M.M. Rahim, P. Chen, A.N. Mottashed, A.B. Mahmoud, M.J. Thomas, Q. Zhu, C.G. Brooks, V. Kartsogiannis, M.T. Gillespie, J.R. Carlyle, and A.P. Makrigiannis The mouse NKR-P1B:Clr-b recognition system is a negative regulator of innate immune responses Blood 125 2015 2217 2227
28. R. Remark, M. Alifano, I. Cremer, A. Lupo, M.C. Dieu-Nosjean, M. Riquet, L. Crozet, H. Ouakrim, J. Goc, A. Cazes, and et al. Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: influence of tumor origin Clin. Cancer Res. 19 2013 4079 4091
29. J. Scheller, C. Garbers, and S. Rose-John Interleukin-6: from basic biology to selective blockade of pro-inflammatory activities Semin. Immunol. 26 2014 2 12
30. A. Steensberg, C.P. Fischer, C. Keller, K. Møller, and B.K. Pedersen IL-6 enhances plasma IL-1ra, IL-10, and cortisol in humans Am. J. Physiol. Endocrinol. Metab. 285 2003 E433 E437
31. K. Taniguchi, and M. Karin IL-6 and related cytokines as the critical lynchpins between inflammation and cancer Semin. Immunol. 26 2014 54 74
32. S.L. Topalian, C.G. Drake, and D.M. Pardoll Immune checkpoint blockade: a common denominator approach to cancer therapy Cancer Cell 27 2015 450 461
33. E. Vivier, S. Ugolini, D. Blaise, C. Chabannon, and L. Brossay Targeting natural killer cells and natural killer T cells in cancer Nat. Rev. Immunol. 12 2012 239 252
34. N.P. Walsh, M. Gleeson, R.J. Shephard, M. Gleeson, J.A. Woods, N.C. Bishop, M. Fleshner, C. Green, B.K. Pedersen, L. Hoffman-Goetz, and et al. Position statement. Part one: Immune function and exercise Exerc. Immunol. Rev. 17 2011 6 63